90 J Cerebrovasc Endovasc Neurosurg Preoperative Embolization of Cerebral Arteriovenous Malformations with Silk Suture and Particles: Technical Considerations and Outcomes Jordan R. Conger 1 , Dale Ding 2 , Daniel M. Raper 2 , Robert M. Starke 3 , Christopher R. Durst 4 , Kenneth C. Liu 2,4 , Mary E. Jensen 4 , Avery J. Evans 4 1 School of Medicine, University of Virginia, Charlottesville, VA, USA 2 Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA 3 Department of Neurological Surgery, University of Miami, Miami, FL, USA 4 Department of Radiology and Medical Imaging, University of Virginia, Charlottesville, VA, USA Objective : Embolization of cerebral arteriovenous malformations (AVMs) is commonly performed prior to surgical resection in order to reduce intra- operative bleeding and improve the safety of resection. Although most modern embolization procedures utilize permanent embolic agents, silk suture and polyvinyl alcohol (PVA) particles may offer unique advantages for preoperative devascularization. The aims of this retrospective cohort study are to describe the technical considerations and determine the outcomes for preoperative silk suture and PVA particle embolization (SPE) of AVMs. Materials and Methods : We performed a retrospective review of our AVM embolization database. AVM patients who underwent preoperative SPE and subsequent surgical resection were included for analysis. Baseline patient demographics, AVM characteristics, embolization and operative records, and post-treatment outcomes were reviewed. Results : A total of 11 patients who underwent 12 preoperative SPE proce- dures were included for analysis. Five AVMs were ruptured (45%), and the median nidus volume was 3.0 cm3 (range: 1.3-42.9 cm 3 ). The Spetzler-Martin grade was I-II in seven patients (64%) and III-IV in four patients (36%). The degree of nidal obliteration was less than 25% in two procedures (17%), 25-50% in one procedure (8%), 50-75% in eight procedures (67%), and greater than 75% in one procedure (8%). The rates of post-emboliza- tion AVM hemorrhage and mortality were 8% and 0%, respectively. The postoperative angiographic obliteration rate was 100%, and the modified Rankin Scale score improved or stable in 91% of patients (median fol- low-up duration 2 months). Conclusion : Preoperative AVM SPE affords a reasonable risk to benefit profile for appropriately selected patients. J Cerebrovasc Endovasc Neurosurg. 2016 June;18(2):90-99 Received : 3 July 2015 Revised : 25 March 2016 Accepted : 30 May 2016 Correspondence to Avery J. Evans Department of Radiology and Medical Imaging, University of Virginia, P.O. Box 800170, VA 22908, USA Tel : 1-434-924-9719 Fax : 1-434-982-3880 E-mail : [email protected]ORCID : http://orcid.org/0000-0002-2627-446X This is an Open Access article distributed under the terms of the Creative Commons Attribution Non- Commercial License (http://creativecommons.org/li- censes/by-nc/3.0) which permits unrestricted non- commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Keywords Endovascular procedures, Intracranial arteriovenous malformation, Intracranial hemorrhages, Microsurgery, Stroke, Vascular malformations Journal of Cerebrovascular and Endovascular Neurosurgery pISSN 2234-8565, eISSN 2287-3139, http://dx.doi.org/10.7461/jcen.2016.18.2.90 Original Article INTRODUCTION Treatment options for cerebral arteriovenous malfor- mations (AVMs) have evolved rapidly over the past
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90 J Cerebrovasc Endovasc Neurosurg
Preoperative Embolization of Cerebral Arteriovenous Malformations with Silk Suture and Particles: Technical Considerations and Outcomes
Jordan R. Conger1, Dale Ding2, Daniel M. Raper2, Robert M. Starke3, Christopher R. Durst4,
Kenneth C. Liu2,4, Mary E. Jensen4, Avery J. Evans4
1School of Medicine, University of Virginia, Charlottesville, VA, USA2Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA3Department of Neurological Surgery, University of Miami, Miami, FL, USA4Department of Radiology and Medical Imaging, University of Virginia, Charlottesville, VA, USA
Objective : Embolization of cerebral arteriovenous malformations (AVMs) is commonly performed prior to surgical resection in order to reduce intra-operative bleeding and improve the safety of resection. Although most modern embolization procedures utilize permanent embolic agents, silk suture and polyvinyl alcohol (PVA) particles may offer unique advantages for preoperative devascularization. The aims of this retrospective cohort study are to describe the technical considerations and determine the outcomes for preoperative silk suture and PVA particle embolization (SPE) of AVMs.
Materials and Methods : We performed a retrospective review of our AVM embolization database. AVM patients who underwent preoperative SPE and subsequent surgical resection were included for analysis. Baseline patient demographics, AVM characteristics, embolization and operative records, and post-treatment outcomes were reviewed.
Results : A total of 11 patients who underwent 12 preoperative SPE proce-dures were included for analysis. Five AVMs were ruptured (45%), and the median nidus volume was 3.0 cm3 (range: 1.3-42.9 cm3). The Spetzler-Martin grade was I-II in seven patients (64%) and III-IV in four patients (36%). The degree of nidal obliteration was less than 25% in two procedures (17%), 25-50% in one procedure (8%), 50-75% in eight procedures (67%), and greater than 75% in one procedure (8%). The rates of post-emboliza-tion AVM hemorrhage and mortality were 8% and 0%, respectively. The postoperative angiographic obliteration rate was 100%, and the modified Rankin Scale score improved or stable in 91% of patients (median fol-low-up duration 2 months).
Conclusion : Preoperative AVM SPE affords a reasonable risk to benefit profile for appropriately selected patients.
J Cerebrovasc Endovasc Neurosurg. 2016 June;18(2):90-99Received : 3 July 2015Revised : 25 March 2016Accepted : 30 May 2016
Correspondence to Avery J. EvansDepartment of Radiology and Medical Imaging, University of Virginia, P.O. Box 800170, VA 22908, USA
Tel : 1-434-924-9719Fax : 1-434-982-3880E-mail : [email protected] : http://orcid.org/0000-0002-2627-446X
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non- Commercial License (http://creativecommons.org/li-censes/by-nc/3.0) which permits unrestricted non- commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
PVA = polyvinyl alcohol; AVM = arteriovenous malformation; mRS= modified Rankin Scale.*mRS determined at latest date after embolization, before surgicalresection.†The complications of hemorrhage and weakness occurred in thesame patient.
Table 2. Embolization outcomes and complications (N = 12)cedures during the study period. Six patients (12 SPE
procedures) were excluded for subsequent treatment
with SRS (four patients) or undergoing surgery at an-
other institution (two patients). This yielded 11 pa-
tients who underwent 12 preoperative SPE proce-
dures for analysis. The patient and AVM character-
istics are summarized in Table 1. Eight patients were
female (73%). The median age of all patients was 32
years (range 13 to 74 years) at the time of initial SPE.
The most frequent clinical symptoms at presentation
were headache and visual deficit, each in eight pa-
tients (72%), sensory deficit in six patients (55%), in-
tracranial hemorrhage (ICH) in five patients (45%;
two cases each of intracerebral and intraventricular
hemorrhage, one case of subarachnoid hemorrhage),
and seizure in three patients (27%). Medical co-
morbidities included smoking in four patients (36%)
and hypertension and hypercholesterolemia each in 3
patients (27%). The mRS scores at presentation were
2 or lower in seven patients (64%) and 3 or greater in
four patients (36%). Three patients (27%) underwent
prior embolization treatment with material other than
silk and PVA particles, and two patients (18%) under-
went prior Gamma Knife SRS.
AVM Characteristics
AVMs were supratentorial in 10 cases (91%). They
were localized to the right side in nine cases (82%), to
the left side in one case (9%), and in the midline in
one case (9%). The most common AVM locations
were occipital in four cases (36%) and frontal in three
cases (27%). Seven nidi were located in eloquent areas
(64%), and seven nidi had a component of deep ve-
nous drainage (64%). The Spetzler-Martin grade was
II in seven patients (64%) and III and IV each in two
patients (18%). AVMs were associated with arterial
and venous aneurysms in six (55%) and five (45%)
cases, respectively.
AVM embolization outcomes with silk suture and
PVA particles
The embolization procedural details and outcomes
are summarized in Table 2. In the 12 SPE procedures,
the degree of AVM obliteration was < 25% in two
cases (17%), 25-50% in one case (8%), 50-75% in eight
cases (67%), and > 75% in one case (8%). The arterial
pedicle was occluded with coils after SPE in seven
Table 3. Microsurgical outcomes and complications (N = 11)
at a median interval of one day (range 1 to 3 days)
after the most recent SPE embolization, the median
estimated intraoperative blood loss was 600 mL
(range 200 to 4,500 mL), and the median operative
duration was 326 minutes (range 237 to 579 minutes).
Based on postoperative angiography (Fig. 1), complete
AVM obliteration was achieved in all cases (100%).
At the most recent clinical follow-up (median dura-
tion 2 months, range 1 to 156.5 months), the mRS
score was 0 in one patient (9%), 1 in four patients
(36%), 2 in two patients (18%), 3 in one patient (9%),
4 in two patients (18%), and 6 in one patient (9%).
Compared to baseline, six patients (55%) showed im-
provement from their mRS score, four patients (36%)
were unchanged, and one patient (9%) worsened.
Postoperative surgical and medical complications in-
cluded visual deficit in five patients (45%), weakness
in two patients (18%), and seizures, sensory changes,
ataxia, urinary tract infection, meningitis, deep vein
thrombosis, and death each in one patient (9%).
Additional interventions performed after AVM re-
section included botulinum toxin chemodenervation
in two patients (18%), and percutaneous endoscopic
gastrostomy tube placement in one patient (9%).
DISCUSSION
Preoperative AVM embolization confers a number
of potential advantages.6)7) By reducing intraoperative
blood loss during AVM surgical resection, preoperative
embolization may improve the safety of these proce-
dures by potentially decreasing the technical difficulty
of resection and operative duration.10) Embolic agents
can be used to mark arterial feeding vessels, which
can be difficult to differentiate from arterialized drain-
ing veins intraoperatively. Preoperative embolization
also devascularizes the deep portions of an AVM ni-
dus, which are difficult to access intraoperatively and
are not typically encountered until the later stages of
AVM dissection. Premature intraoperative hemor-
rhage from the deep portion of a nidus can be diffi-
cult to control. Thus, preoperative embolization may
facilitate AVM circumdissection and extirpation.
In addition to silk suture and PVA particles, cyanoa-
crylates (e.g. NBCA) and Onyx are two embolic agents
used to treat AVMs. NBCA was approved in 2000 af-
ter it was shown to be equivalent to PVA for AVM
embolization.38) While embolization with NBCA may
provide a more thorough and durable nidal devascu-
larization than SPE, NBCA embolization carries a risk
of microcatheter tip entrapment within the embolic
cast, which can precipitate AVM hemorrhage upon for-
cible withdrawal of the microcatheter.8)56) Additionally,
if NBCA is deployed too rapidly, the target artery may
become occluded prior to adequate nidal penetration.
Furthermore, the draining vein can become occluded
before adequate nidal penetration is achieved and ar-
teriovenous shunting is halted, causing a significant
JORDAN R. CONGER ET AL
Volume 18 · Number 2 · June 2016 95
A
B
C
D
E
F
Fig. 1. Cerebral angiography, (A) lateral and (B) AP views of a right internal carotid artery (ICA) injection, shows a 2.9x1.6x1.7 cm ni-dus in the posterior occipitotemporal region with a 7 mm intranidal aneurysm. The arterial supply is from the branches of the right middle cerebral artery (MCA) and posterior cerebral artery (PCA), through an enlarged fetal posterior communicating artery, and venous drainage is strictly superficial into the superior sagittal and right transverse sinuses. This Spetzler-Martin grade II arteriovenous malforma-tion (AVM) was embolized through the right PCA branch feeding artery with 4-0 silk suture, 350-500 ?m polyvinyl alcohol particles, and a single 2x6 hydrocoil. The MCA branch feeder could not be safely embolized due to en passage supply to normal brain parenchyma. Post-embolization angiography, (C) lateral and (D) AP views of a right ICA injection, shows less than 25% AVM devascula-rization, but significantly reduced arterial supply from the embolized PCA branch. Postoperative angiography, (E) lateral and (F) AP views of a right ICA injection, performed six months after surgical resection, shows no evidence of residual nidus.
increase in intranidal pressure, thereby incurring a
much higher risk of rupture.
Onyx is a permanent liquid embolic agent that is
dissolved in dimethyl sulfoxide (DMSO). Once DMSO
diffuses into the blood, Onyx precipitates and leads to
vascular occlusion.53) Although Onyx may provide su-
perior AVM devascularization compared to either
NBCA or silk suture and PVA particles, its risks should
be noted. There have been reports linking DMSO to
vessel necrosis and neuronal swelling.44) Similar to NBCA,
there is also an unavoidable risk of microcatheter en-
trapment with Onyx embolization, although new mi-
crocatheters with detachable tips may lessen the con-
cern for this complication.32)55) Finally, although AVM
embolization with NBCA and Onyx can be curative,
there remains a small risk of recurrence even after
complete angiographic obliteration. Since no single
embolic agent, or combination of agents, has been ac-
cepted as a clear favorite for AVM devascularization,
the nature of each individual nidus and the goals of
embolization should be considered when determining
the embolic agent of choice for a particular case.
PREOPERATIVE AVM EMBOLIZATION WITH SILK SUTURE AND PARTICLES
96 J Cerebrovasc Endovasc Neurosurg
Future developments in endovascular technology may
further improve the safety of modern embolic agents.
In this study, we report the detailed outcomes of 11
AVM patients who underwent 12 preoperative SPE
procedures. The proportion of patients who presented
with AVM rupture was 45%, which is slightly higher
than prior silk suture embolization series.9)45) One pa-
tient, who had a ruptured AVM, experienced post-em-
bolization hemorrhage (8%). In comparison, the rates
of AVM hemorrhage after Onyx embolization are as
high as 12.5% for ruptured, and 1.6% for unruptured
AVMs.32) Although complete AVM occlusion can rare-
ly be achieved with SPE and a significant degree of
devascularization may be challenging for SPE of large
AVMs, the degree of volume reduction was at least
50% for the majority of SPE procedures (75%).
Surgical AVM resection resulted in complete ob-
literation in all patients (100%), with worsened post-
operative mRS in only one patient (9%). Additionally,
64% of patients were functionally independent at a
median follow-up duration of two months. Therefore,
multimodality AVM management with preoperative
SPE and subsequent surgical resection remains a via-
ble combined approach in the modern era.
Reports of AVM embolization with PVA and silk
suture are relatively sparse in the literature, due to an
overall preference for NBCA and Onyx by many
neurointerventionalists. Schmutz et al. reported a ser-
ies in which silk suture was the main embolic agent
in 73 AVM patients, and reported a 1.4% post-emboli-
3. Chen CJ, Chivukula S, Ding D, Starke RM, Lee CC, Yen CP, et al. Seizure outcomes following radiosurgery for cerebral arteriovenous malformations. Neurosurg Focus. 2014 Sep;37(3):E17.
4. Cohen-Inbar O, Ding D, Chen CJ, Sheehan JP. Stereotactic radiosurgery for deep intracranial arteriovenous malfor-mations, part 1: Brainstem arteriovenous malformations. J Clin Neurosci. 2016 Feb;24:30-6.
5. Cohen-Inbar O, Ding D, Sheehan JP. Stereotactic radio-surgery for deep intracranial arteriovenous malformations, part 2: Basal ganglia and thalamus arteriovenous malformations. J Clin Neurosci. 2016 Feb;24:37-42.
6. Crowley RW, Ducruet AF, Kalani MY, Kim LJ, Albuquerque FC, McDougall CG. Neurological morbidity and mortality associated with the endovascular treatment of cerebral arteriovenous malformations before and dur-ing the Onyx era. J Neurosurg. 2015 Jun;122(6):1492-7.
7. Crowley RW, Ducruet AF, McDougall CG, Albuquerque FC. Endovascular advances for brain arteriovenous malformations. Neurosurgery. 2014 Feb;74 Suppl 1:S74-82.
8. Debrun GM, Aletich VA, Shownkeen H, Ausman J. Glued Catheters during Embolisation of Brain AVMs with Acrylic Glue. Interv Neuroradiol. 1997 Mar 30;3(1):13-9.
9. Dehdashti AR, Muster M, Reverdin A, de Tribolet N, Ruefenacht DA. Preoperative silk suture embolization of cerebral and dural arteriovenous malformations. Neurosurg Focus. 2001;11(5):e6.
10. DeMeritt JS, Pile-Spellman J, Mast H, Moohan N, Lu DC, Young WL, et al. Outcome analysis of preoperative embolization with N-butyl cyanoacrylate in cerebral arte-riovenous malformations. AJNR Am J Neuroradiol. 1995 Oct;16(9):1801-7.
11. Ding D, Liu KC. Predictive Capability of the Spetzler-Martin versus supplementary grading scale for microsurgical outcomes of cerebellar arteriovenous malformations. J Cerebrovasc Endovasc Neurosurg. 2013 Dec;15(4):307-10.
12. Ding D, Quigg M, Starke RM, Xu Z, Yen CP, Przybylowski CJ, et al. Radiosurgery for temporal lobe arteriovenous malformations: effect of temporal location on seizure outcomes. J Neurosurg. 2015 Oct;123(4):924-34.
13. Ding D, Quigg M, Starke RM, Yen CP, Przybylowski CJ, Dodson BK, et al. Cerebral arteriovenous malforma-tions and epilepsy, Part 2: predictors of seizure outcomes following radiosurgery. World Neurosurg. 2015 Sep;84(3): 653-62.
14. Ding D, Sheehan JP, Starke RM, Durst CR, Raper DM, Conger JR, et al. Embolization of cerebral arteriovenous malformations with silk suture particles prior to stereotactic radiosurgery. J Clin Neurosci. 2015 Oct;22(10):1643-9.
15. Ding D, Starke RM, Kano H, Lee JY, Mathieu D, Pierce J, et al. Stereotactic radiosurgery for Spetzler-Martin Grade III arteriovenous malformations: an international multicenter study. J Neurosurg. 2016 Apr 15:1-13. [Epub ahead of print]
16. Ding D, Starke RM, Kano H, Mathieu D, Huang P, Kondziolka D, et al. Radiosurgery for cerebral arterio-venous malformations in a randomized trial of unruptured brain arteriovenous malformations (ARUBA)-eligible pa-tients: a multicenter study. Stroke. 2016 Feb;47(2):342-9.
17. Ding D, Starke RM, Liu KC, Crowley RW. Cortical plas-ticity in patients with cerebral arteriovenous malformations. J Clin Neurosci. 2015 Dec;22(12):1857-61.
18. Ding D, Starke RM, Quigg M, Yen CP, Przybylowski CJ, Dodson BK, et al. Cerebral Arteriovenous Malformations and Epilepsy, Part 1: Predictors of Seizure Presentation. World Neurosurg. 2015 Sep;84(3):645-52.
19. Ding D, Starke RM, Yen CP, Sheehan JP. Radiosurgery
PREOPERATIVE AVM EMBOLIZATION WITH SILK SUTURE AND PARTICLES
98 J Cerebrovasc Endovasc Neurosurg
for cerebellar arteriovenous malformations: does infratentorial location affect outcome? World Neurosurg. 2014 Jul-Aug;82 (1-2):e209-17.
20. Ding D, Xu Z, Shih HH, Starke RM, Yen CP, Sheehan JP. Stereotactic radiosurgery for partially resected cerebral arteriovenous malformations. World Neurosurg. 2016 Jan;85:263-72.
21. Ding D, Xu Z, Starke RM, Yen CP, Shih HH, Buell TJ, et al. Radiosurgery for cerebral arteriovenous malformations with associated arterial aneurysms. World Neurosurg. 2016 Mar;87:77-90.
22. Ding D, Xu Z, Yen CP, Starke RM, Sheehan JP. Radiosurgery for cerebral arteriovenous malformations in elderly patients: effect of advanced age on outcomes af-ter intervention. World Neurosurg. 2015 Sep;84(3):795-804.
23. Ding D, Xu Z, Yen CP, Starke RM, Sheehan JP. Radiosurgery for unruptured cerebral arteriovenous mal-formations in pediatric patients. Acta Neurochir (Wien). 2015 Feb;157(2):281-91.
24. Ding D, Yen C, Starke RM, Xu Z, Sheehan JP. Effect of prior hemorrhage on intracranial arteriovenous malfor-mation radiosurgery outcomes. Cerebrovasc Dis. 2014 Dec 24;39(1):53-62.
29. Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for patients with unruptured intracranial arteriovenous malformations. J Neurosurg. 2013 May;118(5):958-66.
30. Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for primary motor and sensory cortex arteriovenous mal-formations: outcomes and the effect of eloquent location. Neurosurgery. 2013 Nov;73(5):816-24.
31. Guglielmi G, Benati A, Perini S. Endovascular emboliza-tion with radiopaque silk threads: a feasibility study in Swine. Interv Neuroradiol. 2006 Jun 15;12(2):109-12.
32. Katsaridis V, Papagiannaki C, Aimar E. Curative embolization of cerebral arteriovenous malformations (AVMs) with Onyx in 101 patients. Neuroradiology. 2008 Jul;50(7):589-97.
33. Kim H, Abla AA, Nelson J, McCulloch CE, Bervini D, Morgan MK, et al. Validation of the supplemented spet-zler-martin grading system for brain arteriovenous mal-formations in a multicenter cohort of 1009 surgical patients. Neurosurgery. 2015 Jan;76(1):25-33.
34. Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL. A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery. 2010 Apr;66(4):702-13; discussion 13.
Overbey JR, et al. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, rand-omised trial. Lancet. 2014 Feb 15;383(9917):614-21.
36. Moosa S, Chen CJ, Ding D, Lee CC, Chivukula S, Starke RM, et al. Volume-staged versus dose-staged ra-diosurgery outcomes for large intracranial arteriovenous malformations. Neurosurg Focus. 2014 Sep;37(3):E18.
37. Mouchtouris N, Jabbour PM, Starke RM, Hasan DM, Zanaty M, Theofanis T, et al. Biology of cerebral arte-riovenous malformations with a focus on inflammation. J Cereb Blood Flow Metab. 2015 Feb;35(2):167-75.
38. n BCATI. N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations: results of a prospective, randomized, multi-center trial. AJNR Am J Neuroradiol. 2002 May;23(5):748-55.
39. Oermann EK, Ding D, Yen CP, Starke RM, Bederson JB, Kondziolka D, et al. Effect of Prior Embolization on Cerebral Arteriovenous Malformation Radiosurgery Outcomes: A Case-Control Study. Neurosurgery. 2015 Sep;77(3):406-17.
40. Oermann EK, Rubinsteyn A, Ding D, Mascitelli J, Starke RM, Bederson JB, et al. Using a Machine Learning Approach to Predict Outcomes after Radiosurgery for Cerebral Arteriovenous Malformations. Sci Rep. 2016 Feb;6:21161.
41. Przybylowski CJ, Ding D, Starke RM, Yen CP, Quigg M, Dodson B, et al. Seizure and anticonvulsant outcomes following stereotactic radiosurgery for intracranial arterio-venous malformations. J Neurosurg. 2015 Jun;122(6):1299-305.
42. Purdy PD, Batjer HH, Risser RC, Samson D. Arteriovenous malformations of the brain: choosing em-bolic materials to enhance safety and ease of excision. J Neurosurg. 1992 Aug;77(2):217-22.
43. Saatci I, Geyik S, Yavuz K, Cekirge HS. Endovascular treatment of brain arteriovenous malformations with pro-longed intranidal Onyx injection technique: long-term re-sults in 350 consecutive patients with completed endo-vascular treatment course. J Neurosurg. 2011 Jul;115(1):78-88.
44. Sampei K, Hashimoto N, Kazekawa K, Tsukahara T, Iwata H, Takaichi S. Histological changes in brain tissue and vasculature after intracarotid infusion of organic solvents in rats. Neuroradiology. 1996 Apr;38(3):291-4.
45. Schmutz F, McAuliffe W, Anderson DM, Elliott JP, Eskridge JM, Winn HR. Embolization of cerebral arterio-venous malformations with silk: histopathologic changes and hemorrhagic complications. AJNR Am J Neuroradiol. 1997 Aug;18(7):1233-7.
46. Schneider BF, Eberhard DA, Steiner LE. Histopathology of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg. 1997 Sep;87(3):352-7.
47. Song JK, Eskridge JM, Chung EC, Blake LC, Elliott JP, Finch L, et al. Preoperative embolization of cerebral ar-teriovenous malformations with silk sutures: analysis and clinical correlation of complications revealed on computerized tomography scanning. J Neurosurg. 2000 Jun;92(6):955-60.
48. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986 Oct;65(4): 476-83.
49. Starke RM, Kano H, Ding D, Lee JY, Mathieu D, Whitesell J, et al. Stereotactic radiosurgery for cerebral arteriovenous malformations: evaluation of long-term outcomes in a
JORDAN R. CONGER ET AL
Volume 18 · Number 2 · June 2016 99
multicenter cohort. J Neurosurg. 2016 Mar 4:1-9. [Epub ahead of print]
50. Starke RM, Sheehan JP, Ding D, Liu KC, Kondziolka D, Crowley RW, et al. Conservative management or intervention for unruptured brain arteriovenous malformations. World Neurosurg. 2014 Nov;82(5):e668-9.
51. Starke RM, Yen CP, Chen CJ, Ding D, Mohila CA, Jensen ME, et al. An updated assessment of the risk of radia-tion-induced neoplasia after radiosurgery of arteriovenous malformations. World Neurosurg. 2014 Sep-Oct;82(3-4):395-401.
52. Starke RM, Yen CP, Ding D, Sheehan JP. A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg. 2013 Oct;119(4):981-7.
53. Taki W, Yonekawa Y, Iwata H, Uno A, Yamashita K, Amemiya H. A new liquid material for embolization of arteriovenous malformations. AJNR Am J Neuroradiol. 1990 Jan-Feb;11(1):163-8.
54. van Beijnum J, van der Worp HB, Buis DR, Al-Shahi Salman R, Kappelle LJ, Rinkel GJ, et al. Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA. 2011 Nov 9;306(18):2011-9.
55. Weber W, Kis B, Siekmann R, Jans P, Laumer R, Kuhne D. Preoperative embolization of intracranial arteriovenous mal-formations with Onyx. Neurosurgery. 2007 Aug;61(2):244-52; discussion 52-4.
56. Wikholm G. Occlusion of cerebral arteriovenous malfor-mations with N-butyl cyano-acrylate is permanent. AJNR Am J Neuroradiol. 1995 Mar;16(3):479-82.
57. Yen CP, Ding D, Cheng CH, Starke RM, Shaffrey M, Sheehan J. Gamma Knife surgery for incidental cerebral arteriovenous malformations. J Neurosurg. 2014 Nov;121(5): 1015-21.